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ORIGINAL ARTICLE
Ahead of print publication  

Obstetric outcomes in antineutrophil cytoplasmic antibody-associated vasculitis: An interview-based study in Northern India


1 Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
2 Department of Clinical and Experimental Sciences, Rheumatology and Immunology Unit, University of Brescia, ASST Spedali Civili, Brescia, Italy

Date of Submission09-Oct-2021
Date of Acceptance17-Mar-2022
Date of Web Publication01-Jul-2022

Correspondence Address:
Latika Gupta,
Department of Clinical Immunology and Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow - 226 014, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/injr.injr_232_21

  Abstract 


Introduction: Rheumatic diseases are associated with poor obstetric outcomes, especially in developing countries. In a multisystem disease like antineutrophil cytoplasmic antibody-associated vasculitis (AAV), pulmonary and renal involvement may contribute to adverse pregnancy outcomes. we explored pregnancy outcomes in women with AAV and compared pregnancies after disease onset to those that occurred before it.
Method: Women with AAV (Chapel Hill Criteria, 2012) registered at a tertiary care center (2001–2021) were interviewed by teleconsultation or during outpatient visits. Maternal complications and fetal complications were recorded.
Results: Median age at disease onset was 48 (33–60) years, with the most common subtype being granulomatosis with polyangiitis (13, 48%) followed by microscopic polyangiitis (10, 37%). Twelve women were in the reproductive age group, of which six suffered from a premature menopause. Three pregnancies in three women after disease onset were compared with 62 pregnancies in 23 women with conception before the disease. Pregnancies before disease onset resulted in 58 (93.3%) live birth. One (33.33%) live birth was observed in the pregnancies after disease onset, and disease onset during pregnancy resulting in intrauterine death at 20 weeks period of gestation. One patient is currently in her antenatal period with no complications so far. This study suggests the absence of impact on pregnancy outcome before diagnosis of AAV.
Conclusion: Pregnancy after a diagnosis of AAV is rare, and successful outcomes may be reported on occasion.

Keywords: Antineutrophil cytoplasmic antibody-associated vasculitis, obstetric outcomes, pregnancy



How to cite this URL:
Gupta L, Mehta P, Kharbanda R, Balakrishnan A, Andreoli L, Agarwal V. Obstetric outcomes in antineutrophil cytoplasmic antibody-associated vasculitis: An interview-based study in Northern India. Indian J Rheumatol [Epub ahead of print] [cited 2022 Dec 5]. Available from: https://www.indianjrheumatol.com/preprintarticle.asp?id=349455




  Introduction Top


Antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis (AAV) is a rare, chronic, disabling, and mandate long-term immunosuppression.[1] At times, these involve women on the childbearing age group, bringing rheumatologists to the cross roads between preserving fertility and managing aggressive disease activity.[2] While lifesaving and timely treatment assume a central role in rheumatology care in such instances, effects of disease and drugs on fertility, pregnancy, and social construct may potentially have an outsized impact on long-term quality of life (QOL) in women with AAV.[3] Since the AAV is rare and often involves men and the elderly, data on effects on obstetric outcomes are rather limited.

End organ damage from AAV, including renal, pulmonary, and neurogenic debility, may be potential contributors to adverse fetal and maternal outcomes.[4] Sexual dysfunction is widely reported in most chronic illnesses[5] and a wide range of rheumatic diseases. Rarely, cutaneous disfigurement from the condition may contribute to poor self-esteem[6] and may indirectly impact sexual health. Notably, a significant disparity in maternal and fetal outcomes is seen in most rheumatic diseases, with some such as myositis adversely impacting fetal outcomes way more than maternal, and vice versa for diseases such as Takayasu arteritis (TAK).[7] Furthermore, the social setting and cultural and financial construct in developing countries may additionally impact outcomes, as previously reported in other rheumatic diseases.

Despite the high risks incurred by chronic diseases, scientific progress in obstetric care including collaborative clinics, ovum banking, and multidisciplinary approach to diligent care holds potential to improve outcomes.[2] Better risk stratification also allows for triage model of healthcare, with greater attention to specific groups for better management. Most previous studies in AAV are limited by few numbers, and a specific understanding of outcomes in developing countries is rather limited.

Adverse obstetric outcomes are expected due to a multitude of factors. Chronic illness can affect fertility, relations, and wish for conception. Overall sexual dysfunction has been reported in women with rheumatic diseases. Capability for childcare is also affected by functional debility.[8] The use of immunosuppressants, some of which are teratogenic, further complicates the issue. Social issues often compound the clinical picture.[9] The exact magnitude of the problem has been explored in a limited number of Indian patients so far. The setting of a developed nation commensurate with associated socio-economic factors is expected to have added impact on obstetric outcomes.[10] India is also culturally diverse and ethnic influences may have a role to play. Knowing obstetric outcomes and understanding of the influencing factors is the first step in measures translating to effort. We have previously identified worse outcomes in idiopathic inflammatory myositis (IIM),[11] systemic sclerosis (SSc),[12] systemic lupus erythematosus,[13] and TAK[7] in Indian patients compared to those in the developed countries.

Thus, the objectives of the present study are to determine whether obstetric outcomes are impacted in patients with AAV, specifically granulomatosis with polyangiitis (GPA), microscopic polyangiitis (MPA), eosinophilic GPA (EGPA), and unclassified form. We also hope to explore the extent of disease impacting maternal and fetal health and compare obstetric outcomes before and after the onset of AAV in Indian women.


  Methods Top


With the above intent, we designed a detail case record form (CRF) for interviewing patients with rare rheumatic diseases.[14] The CRFs were modified to include clinical characteristics specific for different rheumatic diseases.

Patient selection

Women diagnosed with AAV with a vasculitis file based on clinic system were contacted for interview. All women 18 years or older with probable or definite AAV by Chapel Hill Criteria were identified.[15] Data on demographic parameters, clinical profile, and comorbidities were collected from hospital records and supplemented by personal interview between June 2020 and January 2021. Men, patients <18 years, and those unwilling to participate were excluded in this institutional review board certified study (2019–136-IP-EXP-10).

Data collection

We used standard reporting guidelines for survey-based research.[16] The definitions for cases, outcomes, and complications were as previously defined in the published CRF.[14] The key definitions are enlisted here. The questionnaire was recorded by interview over the telephone by a rheumatologist, and the obstetric records were verified using retrospective records in the vasculitis clinic files. The survey development and pilot testing have been detailed before. A detailed workflow chart is depicted as shown in [Figure 1].
Figure 1: A detailed workflow chart

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Disease parameters

Physician's judgment based on clinical and laboratory findings (absence of worsening of disease manifestations and normal laboratory tests and inflammatory markers) was used to define inactive disease.

Antineutrophil cytoplasmic antibody autoantibodies

Data regarding autoantibodies were extracted from the hospital database, and test for autoantibodies ANCA was done using AESKUSLIDES ANCA ethanol (Germany). It determines autoantibodies against c-ANCA, p-ANCA, and atypical ANCA. In addition, CHORUS rapid ELISA is used to test antibodies to proteinase 3 and myeloperoxidase.

Confounding variables

The various confounding factors for adverse pregnancy outcomes, such as prior diabetes, hypertension, any organ disease, maternal parity, maternal age, previous lower segment cesarean section (LSCS), and hypothyroidism, were interviewed about and reviewed.

Obstetric and fertility outcomes

Obstetrics, fertility, contraception use, and social issues were the key areas of exploration. Fertility outcomes included early menopause (defined as presence of sustained amennorrhea for >1 years after attaining menarche, before 40 years of age), deferring pregnancy due to disease process, inability to conceive, and abstinence due to drugs or disease activity. Data on contraception use and social issues were also collected.

Obstetric outcomes were listed as maternal and fetal outcomes. Maternal outcomes included flare of AAV, hypertensive diseases of pregnancy, diabetes, abortions (spontaneous or induced), stillbirths, and live births. Fetal outcomes included prematurity, low birth weight, congenital anomalies, or neonatal deaths. Antiphospholipid antibodies profile of all patients who had pregnancies after disease onset was retrieved.

Statistical analysis

Continuous variables were described as median and interquartile range values. Categorical variables were compared by means of Chi-square test (Fisher's exact test when appropriate) and continuous variables by means of Mann–Whitney U-test. To estimate the effect of disease on various outcomes, the pregnancies before disease onset were taken as controls. The relative risk of different outcomes was calculated. Two mixed generalized models with age, duration of disease, diagnostic category, education status, place of residence, and age at conception as covariates were used to determine the factors influencing maternal and fetal outcomes, respectively. Data were analyzed using SPSS™ 23 software (IBM SPSS Statistics for Windows, Version 23.0. Armonk, NY: IBM Corp).

Comparison with world literature on antineutrophil cytoplasmic antibody-associated vasculitis and healthy population in India

Outcomes reported for a previous study from the United Kingdom (UK, 2015) were compared with the current cohort. Details retrieved from the past 6 years from the Indian population from the United Nations Children's Fund (UNICEF) data ware house[17] were used for comparison with the general population.

Comparison with other rare diseases

Previous studies at our center using similar interview-based methods were conducted for IIM (n = 81),[11] TAK (n = 64),[7] and SSc (n = 15)[12] in the last 5 years. The number of pregnancies after the disease and the respective outcomes were retrieved from these papers and Chi-square test was used to compare outcomes relative to AAV.


  Results Top


Baseline and clinical characteristics

Of 180 patients in the database, after exclusion of men, phone numbers of 45 women were retrieved. Among these, 12 (24%) could not be contacted and 6 (18.2%) deaths were recorded [Figure 1]. A total of 27 patients were thus interviewed.

The median age at diagnosis was 48 (33–60) years with disease duration of 36 (6–84) months. GPA (13/27, 48.1%) was the most common subtype of AAV followed by MPA (10/27, 37%) and EGPA (3/27, 11.1%). Lung involvement was the most common organ involved (20 of 27 cases, 74.1%), of which 8 (8 of 20, 40%) had diffuse alveolar hemorrhage. Nearly half of the patients experienced neurological (48.1%) and renal manifestations (48.1%). Eight (29.6%) patients had ENT involvement and arthritis was reported by 10 (37%) of them [Table 1].
Table 1: Baseline and clinical characteristics

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Among various comorbidities, six (22.2%) patients had diabetes mellitus, seven (25.9%) had hypertension, one (3.7%) had osteoporosis, and two (7.4%) patients each had hypothyroidism and chronic hepatitis B [Table 1].

Antineutrophil cytoplasmic antibody-associated vasculitis auto-antibodies

Autoantibodies were tested in all cases, with nearly half (14, 51.9%) having anti-PR3 specificity. Three cases (11%) were seronegative [Table 1].

Menstrual history and infertility

Menarche was attained at median 13 (13–14) years, and nearly three-fourths (20 of 27, 74.1%) of the women had attained menopause. Of 12 (44.5%) patients in reproductive age group, half (6/12, 50%) suffered a premature menopause.

Contraception use was recorded in two-thirds (4/6, 66.7%). Barrier method (50%) was the most common followed by copper intrauterine device (IUD) and hormonal pills in one (25%) patient each [Supplementary Table 1], with none reporting tubectomy or vasectomy for contraception. Notably, infertility was not reported by any of those interviewed.



Social issues

All the women were married with the exception of two. One (3.7%) did not marry due to disease, while another woman (1, 3.7%) was a widow who did not consider remarriage due to disease.

Obstetric outcomes

A total of 65 pregnancies were recorded in 27 women interviewed. Of these, 62 pregnancies occurred (in 23 women) before the onset of AAV, while 3 pregnancies were recorded (in 3 women) after the onset of the disease, of which one patient is in the second trimester (21 weeks period of gestation [POG]).

Conception before the onset of disease

Of 62 recorded pregnancies, 58 resulted in live births, and 1 each were IUD, neonatal death, spontaneous abortion and MTP. Postpartum hemorrhage (PPH) and pregnancy-induced hypertension (PIH) were reported in 2 (3.2%) females each.

Conception after the onset of disease

Among conceptions after the diagnosis of AAV, one (33.3%) IUD and one (33.3%) live birth were recorded. Disease was in remission in two women at the time of conception, whereas one developed flare of underlying disease mid-pregnancy. One (33.3%) female underwent LSCS for PIH [Table 2].
Table 2: Patient details with conception after disease onset

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Patient characteristic and pregnancy outcomes for conception after disease onset

Three patients had conceived after disease onset. Patient 1 had one uneventful pregnancy 2 years before the disease onset. She had onset of GPA with active disease manifesting as diffuse alveolar hemorrhage during the 16th week of pregnancy which resulted IUD at 20 weeks; despite aggressive management with steroids and intravenous immunoglobulin (IVIG), she attained remission with injection rituximab.

Patient 2 had MPA and achieved remission with EUVAS protocol of cyclophosphamide 1 year before conception, with azathioprine being continued during antenatal period; however, she underwent LSCS at term for PIH and no fetal complications were observed. No postpartum flare was observed in this patient.

Patient 3 had GPA in remission with methotrexate and steroids. However, before planned conception, immunosuppression was changed to azathioprine. She is currently antenatal with 20 weeks POG with no complications observed.

Comparisons between conceptions occurring before and after the onset of antineutrophil cytoplasmic antibody-associated vasculitis

Sixty-two conceptions before AAV were compared with 3 conceptions after the disease onset. Small number of events precluded statistical analysis. However, live births were numerically higher in conception before disease onset (93.5% vs. 33.3%). Notably normal vaginal delivery (NVD) was common in conceptions occurring before disease onset, but not so in those after [Table 3].
Table 3: Comparison of obstetric outcomes before and after the onset of disease

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Comparison with world literature

In comparison to the UK[18] and Canadian cohort,[19] our cohort observed fewer number of live births (90% vs. 33.3%, P = 0.02 and 90% vs. 33.3%, P = 0.04) [Table 4].
Table 4: Comparison with other cohort of antineutrophil cytoplasmic antibody-associated vasculitis and other RDs in the Indian population

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Comparison with healthy Indian population

Records taken from the UNICEF data ware house[17] showed that 17.2% of females had cesarean deliveries in 2015 which is lower in comparison to 33.3% cesarean deliveries in AAV patients.

Comparison with other Rheumatic Disease (RD) in the Indian population

Inflammatory myositis

Obstetric complications and pregnancy outcomes

Obstetrics outcomes of both the cohort were comparable, with similar number of live births being observed (P = 0.75)

Fetal complications

Overall fetal complications of both the cohort were comparable [33.3% vs. 26%, P = 0.36, [Table 4] and [Figure 2]].
Figure 2: Pregnancy outcomes in various rheumatic diseases

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Systemic sclerosis

Obstetric complications and pregnancy outcomes

Number of live births in both the groups was similar (P = 0.41)

Fetal complications

Overall fetal complications of both the cohort were similar [P = 0.83, [Table 4] and [Figure 2]].

Takayasu arteritis

Obstetric outcomes and pregnancy outcomes

Live births recorded in TAK cohort were higher than our cohort (73% vs. 33.3%) but not statistically significant (P = 0.12)

Fetal complications

Fetal complications were similar in our cohort when compared to TAK [P = 0.79, [Table 4] and [Figure 2]].


  Discussion Top


In this study from a tertiary care center in Northern India, we found that majority of women were postmenopausal at the time of disease onset. For those in the reproductive age group, premature menopause was common. Pregnancy after the onset of AAV was uncommon and was marred by fewer live births and lower chances of a NVD. The live births observed were fewer in comparison with studies from developed countries but comparable with those in other RDs in Indian women. The prognosis of patients with AAV has improved significantly over the past few decades.[4] With improving disease-free survival, other domains affecting QOL, such as fertility and pregnancy, are assuming a larger role in patient care.

Although fewer numbers preclude a direct comparison, when cohorts from the UK and Canada were reviewed, pregnancy outcomes were less favorable in our cohort with respect to live births and maternal complications. However, the overall rate of fetal complications and cesarean section were similar across the three cohorts. This could be attributed to better maternal and child health facilities in developed nations.

AAV itself is rare and manifests in the middle aged and elderly, at a time when patients are beyond their reproductive age. Our observations were aligned with previous data, with a median age of disease onset in the late forties.[20] Notably, this is younger than reported form other centers as the Indian population dynamics poses a younger age of onset of rheumatic diseases. A recent systematic review reported merely 57 reports describing 131 conception events.[4] The entire spectrum of maternal and fetal complications were reported; however, normal vaginal deliveries were seen in 116 cases, suggesting a possibility of better outcomes with diligent multidisciplinary care. The subsequent step in understanding outcomes is comparing datasets from developed and developing countries, to identify areas of unmet need and potential improvement in rheumatologic–obstetric care. Poor overall maternal and child health, owing to poor facilities especially in rural areas, delayed diagnosis, financial barriers, and socio-cultural constructs, further hampers more delicate care required with conception on a background of a chronic disease.

Another important issue to consider is low rate of conception after development of disease. Three of six women in the reproductive age group suffered from a premature menopause. As older treatment regimens were based on intensive use of cyclophosphamide for induction, this predisposed woman to premature ovarian failure. Although use of cyclophosphamide in young women with lupus has not shown to affect fertility adversely, women with AAV tend to be older predisposing them to a diminished ovarian reserve.[21],[22] The last decade has shown promising outcomes with rituximab-based induction and maintenance regimens; they being recommended now over cyclophosphamide as first line drugs in AAV.[23],[24] Availability of biosimilars with reduced cost and similar efficacy, offers to be the preferred option in women with AAV, especially in the reproductive age group.[25]

It is noteworthy that contraception use was poor in our study in the few women who were in the fertile age group. This mirrors previous observations in other RDs, reiterating the need to educate and empower patients to manage their sexual health. Sex education may be imparted early on in the disease, as well as in a broader approach in school curricula. Adjunct counseling clinics, as well as sexual health clinics, may impart the necessary education to educate the patients as well as (more importantly their kin), in an effort to increase awareness and reduce stigmatization associated with chronic diseases. Sexual dysfunction of any kind is known to be associated with depression in vasculitis.[26] Such issues often remain unaddressed and not discussed in households in certain cultures, increasing the impact of sextual health on QOL in AAV, among other RDs. Similar observations have been reported from Latin American countries, calling for action on this front for better obstetric and rheumatologic care.[27]

Some diseases like IIM have a disproportionately worse maternal than fetal outcomes. In TA, abdominal aortic involvement predisposed to hypertension as an important complication. Hypertension was also reported in 21% in the recent systematic review in AAV. Overall, the results are inconclusive in terms of direct comparability with other RDs, with the need to systematically study outcomes in rare RDs, especially in developing countries.

Another important aspect is managing disease during pregnancy. Notably, one of our cases was diagnosed with AAV during pregnancy. Precious pregnancy and AAV together can pose a major challenge for the clinician. Previously, IVIG has been used successfully in these with good outcomes, as in the current case.[28] Notably, most of our cases who got pregnant also had severe forms of disease, including Diffuse alveolar haemorrhage (DAH), which may mandate PLEX. A recent systematic review examined PLEX for AAV but excluded women who were pregnant.[29] Azathioprine is considered safe for maintenance. Antenatal exposure to Rituximab has been reported to be safe in terms of fetal complications and congenital malformations. Plausible risk of spontaneous abortions and neonatal infections was a concern.[30],[31] Case reports describing the use of tacrolimus in AAV have been published, but the data are limited.[32]

Thus, preconceptional planning to ensure drug safety, early disclosure of pregnancy to all caregivers including the rheumatologist, family physician, obstetrician, and maternal–fetal medicine specialist, and planning of safe medication use and treatment plan for acute flares and disease management peripartum and postpartum with an adequate financial back up and neonatal intensive care unit backup cannot be reiterated enough.[33],[34],[35] Thrombotic events are another concern in these patients.[36],[37]

We have few limitations inherent to studying rare diseases. Small sample size with very few events and an interview-based design with intrinsic recall bias are the two prime drawbacks of our study. To study a larger sample size with a prospective design will help fill the lacunae in our analysis of obstetric outcomes in AAV in the future.


  Conclusion Top


Majority of women were postmenopausal at the time of disease onset, and for those in the reproductive age group, premature menopause was common. Fetal complications and risk of cesarean delivery were higher in the live births observed after disease onset. The prognosis of patients with AAV has improved significantly over the past few decades and with improving disease-free survival, other domains affecting QOL, such as fertility and pregnancy assume a greater importance in giving holistic patient care.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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[PUBMED]  [Full text]  
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